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Genetic Recombination at the Buff Spore Color Locus in Sordaria Brevicollis

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Genetic Recombination at the Buff Spore Color Locus in Sordaria Brevicollis Copyright 0 1983 by the Genetics Society of America GENETIC RECOMBINATION AT THE BUFF SPORE COLOR LOCUS IN SORDARIA BREVICOLLIS. 11. ANALYSIS OF FLANKING MARKER BEHAVIOR IN CROSSES BETWEEN BUFF MUTANTS HELEN SANG' AND HAROLD L. K. WHITEHOUSE Botany School, University of Combridge, Cambridge, England Manuscript received February 24, 1982 Revised copy accepted July 21, 1982 ABSTRACT Aberrant asci containing one or more wild-type spores were selected from crosses between pairs of alleles of the buff locus in the presence of closely linked flanking markers. Data were obtained relating to the site of aberrant segregation and the position of any associated crossover giving recombination of flanking markers. Aberrant segregation at a proximal site within the buff gene may be associated with a crossover proximal to the site of aberrant segregation or, with equal frequency, with a crossover distal to the site of the second mutant present in the cross. Similarly, segregation at a distal site may be associated with a crossover distal to the site or, with lower frequency, with a crossover proximal to the site of the proximal mutant present in the cross. Crossovers between the alleles were rare. This evidence for the relationship between hybrid DNA and crossing over is discussed in terms of current models for the mechanism of recombination. URRENT models of the mechanism of genetic recombination consider gene C conversion and crossing over to be consequences of the same primary event. The MESELSONand RADDING(1975) model proposes that hybrid DNA formation is initiated asymmetrically outside a gene by single-strand transfer between paired homologues. Hybrid DNA forms on one chromatid and moves into the gene. This can lead to postmeiotic segregation and conversion at any nonhomologous sites included in the heteroduplex. Strand isomerization can take place after dissociation of the enzyme to give recombinant flanking markers if the two crossed strands are cut. The hybrid DNA may move through the gene by rotary diffusion, generating symmetrical hybrid DNA as in the HOLLIDAY (1964) model. Cutting of equivalent pairs of crossed strands will give parental or recombinant chromatid arms, depending on whether or not isomerization has occurred. The MESELSONand RADDINGmodel predicts a gradient of asymmetric events, decreasing from the site of initiation of hybrid DNA, and a corresponding increase in symmetric events. This prediction is supported by the data from the Present address: Department of Molecular Biology, Edinburgh University, King's Buildings, Mayfield Road, Edinburgh, Scotland. Genetics 103 161-178 February, 1983. 162 H. SANG AND H. L. K. WHITEHOUSE b2 locus of Ascobolus immersus obtained by PAQUETTEand ROSSIGNOL(1978) and ROSSIGNOL, PAQUETTE and NICOLAS(1978). The model also has implications for the position of crossovers in relation to hybrid DNA. Crossovers are predicted to occur at the distal end of the hybrid DNA, if its formation is initiated on the proximal side of the gene, and, conversely, at the proximal end, if the event is initiated on the distal side of the gene. Hybrid DNA is continuous between the site of initiation and a crossover. The relationship between gene conversion and crossing over can be investi- gated to some extent by analyzing outside marker behavior associated with gene conversion at a linked site. More information can be obtained by a detailed study of interallelic recombination. Interallelic recombination in fungi is not usually caused by classical crossing over between two alleles. It is a result of nonreciprocal events. FOGELand HURST(1967) studied flanking marker behavior in relation to gene conversion at the histidine-1 locus of Saccharomyces cere- visiae. SAVAGEand HASTINGS(1981) obtained further data from this locus. Comparable results for the grey gene of Sordaria fimicola are given by KITANI and WHITEHOUSE(1974). We describe here results from two-point crosses at the buff locus of Sordaria brevicollis with outside markers present. SANGand WHITEHOUSE(1979) de- scribed the results of crosses between buff mutants and wild type using the same flanking markers. We concluded that hybrid DNA formation giving aberrant segregation at buff was mainly asymmetric. The frequency of recom- bination associated with aberrant segregation was significantly less than 50%. The recombination frequency was lower for odd-ratio aberrant asci than for even-ratio asci. The study described here was carried out to analyze the relationship between aberrant segregation and crossing over in more detail. These results are compared with those from the similar studies. The implications for models of the mechanism of recombination are discussed. MATERIALS AND MET~DS (a) Mutants: The buff gene is located about 4 map units from the centromere in the right arm of linkage group I1 of S. brevicollis. The buff mutants used were three ultraviolet-induced mutants, YS9, C47 and C67, and one ethylmethanesulfonate-induced mutant, YS132. Analysis of these mutants in one-point crosses has been described by SANGand WHITEHOUSE(1979). Each mutant has a characteristic conversion pattern. C47, C67 and YS232 give both postmeiotic segregation and conversion aberrant asci in crosses to wild type. Throughout this paper where ratios of wild-type and mutant spores are given the number of wild-type spores is written first and the number of mutant second, e.g., six wild type: two mutant is given as 62. YS9 gives mainly 6:2 aberrant asci. C47 is the most proximal mutant, and C67 is the most distal, according to our results and those reported by MACDONALDand WHITEHOUSE(1979). The criteria for mapping the alleles were the relative frequencies of the two recombinant flanking marker genotypes in wild-type recombinants from pairwise crosses of the mutants in trans. The relative positions of YS132 and YS9 are uncertain. The flanking markers used were met-1, a methionine-requiring mutant, and nic-2, a nicotinamide- requiring mutant described by MACDONALDand WHITEHOUSE(1979) and BOND crosses postmeiotic segregation and conversion occur more frequently at gene (BOND1973; MACDONALDand WHITEHOUSE1979). GENETIC RECOMBINATION IN SORDARIA 163 (b) Culture media: Grossing, germination and minimal media were as defined by FIELDSand OUVS(1967). Minimal medium supplemented with 0.01 &liter of nicotinamide or methionine was used to test for the auxotrophic markers. (c) Method: Crosses were made between pairs of buff mutants and cultured at 30° for 8 days. The general cross was met-1 1 + + X + + 2 nic-1. In all crosses analyzed C67 was the distal (2) allele. C67 is darker than the other mutants and has a higher germination frequency. This effect is not autonomous. All spores from a cross between C67 and another buff allele show increased germination. This is a great advantage in analyzing asci from two-point crosses as poor germination would make complete octad analysis difficult. Asci containing one or more wild-type spores were selected from squash preparations of ascal clusters in 8% glucose solution. The spores were dissected out and allowed to germinate at 37" for approximately 6 hr. The resulting single-spore cultures were tested to determine the flanking marker configuration and backcrossed to both buff mutant parents to identify the buff alleles present. Only a limited number of buff spores were scored for the buff alleles present. Two studies were undertaken. The first was to ascertain the position of the crossover giving flanking-marker recombination, as far as possible, in relation to aberrant segregation within the buff gene. The second set of experiments was done to give an estimate of the extent of hybrid DNA in buff, particularly to find if both alleles or only one were included in hybrid DNA. In the first set of experiments the buff allele was identified only in buff spores with marker recombination. In the second set of experiments only 1:7 asci were analyzed, but the genotype of the buff sister spore to the single wild-type spore was determined for all asci. RESULTS 1. Classification of asci: In the first experiment the asci were classified in terms of 1:7 or 2:6 segregation, the allele that showed aberrant segregation and flanking marker configuration. The chromatids involved in any aberrant seg- regation or crossover events and the locations of crossovers were also deter- mined. Possible crossover locations are shown in Figure 1. For 1:7 asci the position of the crossover can be localized, as at either x or z (Figure l), provided the hybrid DNA is confined to one chromatid. The need for hybrid DNA to be asymmetric is illustrated in Table 1where 5:3 segregation at X Y 2 1 + m + + n -4- 2 FIGURE1.-Possible crossover positions in a two-point cross with flanking markers present. 164 H. SANG AND H. L. K. WHITEHOUSE TABLE 1 Crossover Jocalization with asymmetric or symmetric hybrid DNA formation Position of crossover (Figure 1) Parental X Y (A) m 1 + + m 1 ++ m 1 + + m 1/+ + + m+ 2 n m 1/+ 2 n + + 2 n + I/+ + + + + ++ + + 2 n + + 2 n + + 2 n Tritype (B) m1+ + m 1 + + m 1 ++ m++ + m 1/+ 2 n m+ 2 n + 1/+ 2 n + +++ + 1/+ + + + + 2 n + + 2 n + + 2 n Tetratype Ascus genotypes that result from crossing over adjacent to a mutant showing 5:3 segregation when a second allele shows normal 4:4 segregation. In (A) the hybrid DNA could be confined to one chromatid (asymmetric), but in (B) it involves both (symmetric). the proximal site is considered. If the aberrant segregation results from hybrid DNA in one chromatid only, two of the four products of meiosis will have the same genotype in a noncrossover ascus, giving a tritype ascus (Table 1). The corresponding genotypes with a crossover at x or y (Figure 1) are shown in the table. If the 5:3 segregation results from hybrid DNA in both chromatids, there will have been mismatch correction to wild type in one chromatid but not the other.
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